Modeling neurodegenerative diseases in Caenorhabditis elegans

Experimental Neurology

Volumn 250, Issue , 2013, Pages 94-103

  Li, Jia ^a   Le, Weidong ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

Alzheimer's disease (AD); Amyotrophic lateral sclerosis (ALS); Caenorhabditis elegans; Huntington's disease (HD); Model organism; Neurodegeneration; Parkinson's disease (PD)

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; DJ 1 PROTEIN; HUNTINGTIN; LEUCINE RICH REPEAT KINASE 2; PARKIN; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE PINK1; TAR DNA BINDING PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ABETA GENE; AMYOTROPHIC LATERAL SCLEROSIS; CAENORHABDITIS ELEGANS; DEGENERATIVE DISEASE; DISEASE MODEL; DJ 1 GENE; GENE; GENE IDENTIFICATION; GENE INTERACTION; GENETIC ASSOCIATION; HTT GENE; HUNTINGTON CHOREA; LRRK2 GENE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PARKIN GENE; PARKINSON DISEASE; PINK1 GENE; PRIORITY JOURNAL; REVIEW; SNCA GENE; SOD1 GENE; TAU GENE; TDP 43 GENE; TRANSGENIC ORGANISM; UNC 54 GENE;

ALZHEIMER'S DISEASE (AD); AMYOTROPHIC LATERAL SCLEROSIS (ALS); CAENORHABDITIS ELEGANS; HUNTINGTON'S DISEASE (HD); MODEL ORGANISM; NEURODEGENERATION; PARKINSON'S DISEASE (PD);

ANIMALS; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; HUMANS; NEURODEGENERATIVE DISEASES;

EID: 84885763064     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.09.024     Document Type: Review

References (109)

1. Alavez S., Vantipalli M.C., Zucker D.J., Klang I.M., Lithgow G.J. Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 2011, 472:226-229.
2. Ash P.E., Zhang Y.J., Roberts C.M., Saldi T., Hutter H., Buratti E., Petrucelli L., Link C.D. Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum. Mol. Genet. 2010, 19:3206-3218.
3. Bertram L., Lill C.M., Tanzi R.E. The genetics of Alzheimer disease: back to the future. Neuron 2010, 68:270-281.
4. Boccitto M., Lamitina T., Kalb R.G. Daf-2 signaling modifies mutant SOD1 toxicity in C. elegans. PLoS One 2012, 7:e33494.
5. Bonifati V., Oostra B.A., Heutink P. Linking DJ-1 to neurodegeneration offers novel insights for understanding the pathogenesis of Parkinson's disease. J. Mol. Med. (Berl.) 2004, 82:163-174.
6. Bonifati V., Rohe C.F., Breedveld G.J., Fabrizio E., De Mari M., Tassorelli C., Tavella A., Marconi R., Nicholl D.J., Chien H.F., Fincati E., Abbruzzese G., Marini P., De Gaetano A., Horstink M.W., Maat-Kievit J.A., Sampaio C., Antonini A., Stocchi F., Montagna P., Toni V., Guidi M., Dalla Libera A., Tinazzi M., De Pandis F., Fabbrini G., Goldwurm S., de Klein A., Barbosa E., Lopiano L., Martignoni E., Lamberti P., Vanacore N., Meco G., Oostra B.A., Italian Parkinson Genetics Network Early-onset Parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology 2005, 65:87-95.
7. Brandt R., Gergou A., Wacker I., Fath T., Hutter H. A Caenorhabditis elegans model of tau hyperphosphorylation: induction of developmental defects by transgenic overexpression of Alzheimer's disease-like modified tau. Neurobiol. Aging 2009, 30:22-33.
8. Brignull H.R., Moore F.E., Tang S.J., Morimoto R.I. Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. J. Neurosci. 2006, 26:7597-7606.
9. Cao S., Gelwix C.C., Caldwell K.A., Caldwell G.A. Torsin-mediated protection from cellular stress in the dopaminergic neurons of Caenorhabditis elegans. J. Neurosci. 2005, 25:3801-3812.
10. Chen S., Sayana P., Zhang X.J., Le W. Genetics of amyotrophic lateral sclerosis: an update. Molecular Neurodegeration. 2013, 8(1):28.
11. Cohen E., Bieschke J., Perciavalle R.M., Kelly J.W., Dillin A. Opposing activities protect against age-onset proteotoxicity. Science 2006, 313:1604-1610.
12. Cooper A.A., Gitler A.D., Cashikar A., Haynes C.M., Hill K.J., Bhullar B., Liu K., Xu K., Strathearn K.E., Liu F., Cao S., Caldwell K.A., Caldwell G.A., Marsischky G., Kolodner R.D., Labaer J., Rochet J.C., Bonini N.M., Lindquist S. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006, 313:324-328.
13. Culetto E., Sattelle D.B. A role for Caenorhabditis elegans in understanding the function and interactions of human disease genes. Hum. Mol. Genet. 2000, 9:869-877.
14. Daigle I., Li C. apl-1, a Caenorhabditis elegans gene encoding a protein related to the human beta-amyloid protein precursor. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:12045-12049.
15. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., Jiang H., Hirano M., Rampersaud E., Jansen G.H., Donkervoort S., Bigio E.H., Brooks B.R., Ajroud K., Sufit R.L., Haines J.L., Mugnaini E., Pericak-Vance M.A., Siddique T. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
16. Dickey C.A., Yue M., Lin W.L., Dickson D.W., Dunmore J.H., Lee W.C., Zehr C., West G., Cao S., Clark A.M., Caldwell G.A., Caldwell K.A., Eckman C., Patterson C., Hutton M., Petrucelli L. Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species. J. Neurosci. 2006, 26:6985-6996.
17. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997, 277:1990-1993.
18. Diomede L., Cassata G., Fiordaliso F., Salio M., Ami D., Natalello A., Doglia S.M., De Luigi A., Salmona M. Tetracycline and its analogues protect Caenorhabditis elegans from beta amyloid-induced toxicity by targeting oligomers. Neurobiol. Dis. 2010, 40:424-431.
19. Dostal V., Roberts C.M., Link C.D. Genetic mechanisms of coffee extract protection in a Caenorhabditis elegans model of beta-amyloid peptide toxicity. Genetics 2010, 186:857-866.
20. Faber P.W., Alter J.R., MacDonald M.E., Hart A.C. Polyglutamine-mediated dysfunction and apoptotic death of a Caenorhabditis elegans sensory neuron. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:179-184.
21. Faber P.W., Voisine C., King D.C., Bates E.A., Hart A.C. Glutamine/proline-rich PQE-1 proteins protect Caenorhabditis elegans neurons from huntingtin polyglutamine neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:17131-17136.
22. Fatouros C., Pir G.J., Biernat J., Koushika S.P., Mandelkow E., Mandelkow E.M., Schmidt E., Baumeister R. Inhibition of tau aggregation in a novel Caenorhabditis elegans model of tauopathy mitigates proteotoxicity. Hum. Mol. Genet. 2012, 21:3587-3603.
23. Fay D.S., Fluet A., Johnson C.J., Link C.D. In vivo aggregation of beta-amyloid peptide variants. J. Neurochem. 1998, 71:1616-1625.
24. Fonte V., Kapulkin V., Taft A., Fluet A., Friedman D., Link C.D. Interaction of intracellular beta amyloid peptide with chaperone proteins. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9439-9444.
25. Fonte V., Kipp D.R., Yerg J., Merin D., Forrestal M., Wagner E., Roberts C.M., Link C.D. Suppression of in vivo beta-amyloid peptide toxicity by overexpression of the HSP-16.2 small chaperone protein. J. Biol. Chem. 2008, 283:784-791.
26. Friedman L.G., Lachenmayer M.L., Wang J., He L., Poulose S.M., Komatsu M., Holstein G.R., Yue Z. Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of alpha-synuclein and LRRK2 in the brain. J. Neurosci. 2012, 32:7585-7593.
27. Gidalevitz T., Ben-Zvi A., Ho K.H., Brignull H.R., Morimoto R.I. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 2006, 311:1471-1474.
28. Gidalevitz T., Krupinski T., Garcia S., Morimoto R.I. Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet. 2009, 5:e1000399.
29. Gitler A.D., Chesi A., Geddie M.L., Strathearn K.E., Hamamichi S., Hill K.J., Caldwell K.A., Caldwell G.A., Cooper A.A., Rochet J.C., Lindquist S. Alpha-synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat. Genet. 2009, 41:308-315.
30. Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell 1993, 72:971-983.
31. Guthrie C.R., Greenup L., Leverenz J.B., Kraemer B.C. MSUT2 is a determinant of susceptibility to tau neurotoxicity. Hum. Mol. Genet. 2011, 20:1989-1999.
32. Hamamichi S., Rivas R.N., Knight A.L., Cao S., Caldwell K.A., Caldwell G.A. Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:728-733.
33. Hardy J. Genetic analysis of pathways to Parkinson disease. Neuron 2010, 68:201-206.
34. Harrington A.J., Yacoubian T.A., Slone S.R., Caldwell K.A., Caldwell G.A. Functional analysis of VPS41-mediated neuroprotection in Caenorhabditis elegans and mammalian models of Parkinson's disease. J. Neurosci. 2012, 32:2142-2153.
35. Hassan W.M., Merin D.A., Fonte V., Link C.D. AIP-1 ameliorates beta-amyloid peptide toxicity in a Caenorhabditis elegans Alzheimer's disease model. Hum. Mol. Genet. 2009, 18:2739-2747.
36. Huang Y., Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148:1204-1222.
37. Kalia L.V., Kalia S.K., McLean P.J., Lozano A.M., Lang A.E. alpha-Synuclein oligomers and clinical implications for Parkinson disease. Ann. Neurol. 2013, 73:155-169.
38. Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 1993, 366:461-464.
39. Kimura K.D., Tissenbaum H.A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997, 277:942-946.
40. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile Parkinsonism. Nature 1998, 392:605-608.
41. Klein C., Westenberger A. Genetics of Parkinson's disease. Cold Spring Harb. Perspect. Med. 2012, 2:a008888.
42. Kraemer B.C., Schellenberg G.D. SUT-1 enables tau-induced neurotoxicity in C. elegans. Hum. Mol. Genet. 2007, 16:1959-1971.
43. Kraemer B.C., Zhang B., Leverenz J.B., Thomas J.H., Trojanowski J.Q., Schellenberg G.D. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9980-9985.
44. Kraemer B.C., Burgess J.K., Chen J.H., Thomas J.H., Schellenberg G.D. Molecular pathways that influence human tau-induced pathology in Caenorhabditis elegans. Hum. Mol. Genet. 2006, 15:1483-1496.
45. Kuwahara T., Koyama A., Gengyo-Ando K., Masuda M., Kowa H., Tsunoda M., Mitani S., Iwatsubo T. Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans. J. Biol. Chem. 2006, 281:334-340.
46. Kuwahara T., Koyama A., Koyama S., Yoshina S., Ren C.H., Kato T., Mitani S., Iwatsubo T. A systematic RNAi screen reveals involvement of endocytic pathway in neuronal dysfunction in alpha-synuclein transgenic C. elegans. Hum. Mol. Genet. 2008, 17:2997-3009.
47. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., Davis A., Gilchrist J., Kasarskis E.J., Munsat T., Valdmanis P., Rouleau G.A., Hosler B.A., Cortelli P., de Jong P.J., Yoshinaga Y., Haines J.L., Pericak-Vance M.A., Yan J., Ticozzi N., Siddique T., McKenna-Yasek D., Sapp P.C., Horvitz H.R., Landers J.E., Brown R.H. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
48. Lakso M., Vartiainen S., Moilanen A.M., Sirvio J., Thomas J.H., Nass R., Blakely R.D., Wong G. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J. Neurochem. 2003, 86:165-172.
49. Lee V.M., Goedert M., Trojanowski J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 2001, 24:1121-1159.
50. Lee J.Y., Song J., Kwon K., Jang S., Kim C., Baek K., Kim J., Park C. Human DJ-1 and its homologs are novel glyoxalases. Hum. Mol. Genet. 2012, 21:3215-3225.
51. Lejeune F.X., Mesrob L., Parmentier F., Bicep C., Vazquez-Manrique R.P., Parker J.A., Vert J.P., Tourette C., Neri C. Large-scale functional RNAi screen in C. elegans identifies genes that regulate the dysfunction of mutant polyglutamine neurons. BMC Genomics 2012, 13:91.
52. Li J., Huang K.X., Le W.D. Establishing a novel C. elegans model to investigate the role of autophagy in amyotrophic lateral sclerosis. Acta Pharmacol. Sin. 2013, 34:644-650.
53. Liachko N.F., Guthrie C.R., Kraemer B.C. Phosphorylation promotes neurotoxicity in a Caenorhabditis elegans model of TDP-43 proteinopathy. J. Neurosci. 2010, 30:16208-16219.
54. Liachko N.F., McMillan P.J., Guthrie C.R., Bird T.D., Leverenz J.B., Kraemer B.C. CDC7 inhibition blocks pathological TDP-43 phosphorylation and neurodegeneration. Ann. Neurol. 2013, 74:39-52.
55. Lim M.A., Selak M.A., Xiang Z., Krainc D., Neve R.L., Kraemer B.C., Watts J.L., Kalb R.G. Reduced activity of AMP-activated protein kinase protects against genetic models of motor neuron disease. J. Neurosci. 2012, 32:1123-1141.
56. Link C.D. Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9368-9372.
57. Link C.D., Taft A., Kapulkin V., Duke K., Kim S., Fei Q., Wood D.E., Sahagan B.G. Gene expression analysis in a transgenic Caenorhabditis elegans Alzheimer's disease model. Neurobiol. Aging 2003, 24:397-413.
58. Liu Z., Hamamichi S., Lee B.D., Yang D., Ray A., Caldwell G.A., Caldwell K.A., Dawson T.M., Smith W.W., Dawson V.L. Inhibitors of LRRK2 kinase attenuate neurodegeneration and Parkinson-like phenotypes in Caenorhabditis elegans and Drosophila Parkinson's disease models. Hum. Mol. Genet. 2011, 20:3933-3942.
59. Long Y.C., Zierath J.R. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest. 2006, 116:1776-1783.
60. Markaki M., Tavernarakis N. Modeling human diseases in Caenorhabditis elegans. Biotechnol. J. 2010, 5:1261-1276.
61. McCormick A.V., Wheeler J.M., Guthrie C.R., Liachko N.F., Kraemer B.C. Dopamine D2 receptor antagonism suppresses tau aggregation and neurotoxicity. Biol. Psychiatry 2013, 73:464-471.
62. Miyasaka T., Ding Z., Gengyo-Ando K., Oue M., Yamaguchi H., Mitani S., Ihara Y. Progressive neurodegeneration in C. elegans model of tauopathy. Neurobiol. Dis. 2005, 20:372-383.
63. Murakami T., Yang S.P., Xie L., Kawano T., Fu D., Mukai A., Bohm C., Chen F., Robertson J., Suzuki H., Tartaglia G.G., Vendruscolo M., Kaminski Schierle G.S., Chan F.T., Moloney A., Crowther D., Kaminski C.F., Zhen M., St George-Hyslop P. ALS mutations in FUS cause neuronal dysfunction and death in Caenorhabditis elegans by a dominant gain-of-function mechanism. Hum. Mol. Genet. 2012, 21:1-9.
64. Nass R., Hall D.H., Miller D.M., Blakely R.D. Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3264-3269.
65. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
66. Oeda T., Shimohama S., Kitagawa N., Kohno R., Imura T., Shibasaki H., Ishii N. Oxidative stress causes abnormal accumulation of familial amyotrophic lateral sclerosis-related mutant SOD1 in transgenic Caenorhabditis elegans. Hum. Mol. Genet. 2001, 10:2013-2023.
67. Orenstein S.J., Kuo S.H., Tasset I., Arias E., Koga H., Fernandez-Carasa I., Cortes E., Honig L.S., Dauer W., Consiglio A., Raya A., Sulzer D., Cuervo A.M. Interplay of LRRK2 with chaperone-mediated autophagy. Nat. Neurosci. 2013, 16:394-406.
68. Paisan-Ruiz C., Jain S., Evans E.W., Gilks W.P., Simon J., van der Brug M., Lopez de Munain A., Aparicio S., Gil A.M., Khan N., Johnson J., Martinez J.R., Nicholl D., Carrera I.M., Pena A.S., de Silva R., Lees A., Marti-Masso J.F., Perez-Tur J., Wood N.W., Singleton A.B. Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 2004, 44:595-600.
69. Parker J.A., Connolly J.B., Wellington C., Hayden M., Dausset J., Neri C. Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13318-13323.
70. Parker J.A., Arango M., Abderrahmane S., Lambert E., Tourette C., Catoire H., Neri C. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 2005, 37:349-350.
71. Poorkaj P., Nutt J.G., James D., Gancher S., Bird T.D., Steinbart E., Schellenberg G.D., Payami H. Parkin mutation analysis in clinic patients with early-onset Parkinson [corrected] disease. Am. J. Med. Genet. A 2004, 129A:44-50.
72. Pu P., Le W. Dopamine neuron degeneration induced by MPP+ is independent of CED-4 pathway in Caenorhabditis elegans. Cell Res. 2008, 18:978-981.
73. Rademakers R., Neumann M., Mackenzie I.R. Advances in understanding the molecular basis of frontotemporal dementia. Nat. Rev. Neurol. 2012, 8:423-434.
74. Rebolledo D.L., Aldunate R., Kohn R., Neira I., Minniti A.N., Inestrosa N.C. Copper reduces Abeta oligomeric species and ameliorates neuromuscular synaptic defects in a C. elegans model of inclusion body myositis. J. Neurosci. 2011, 31:10149-10158.
75. Recchia A., Debetto P., Negro A., Guidolin D., Skaper S.D., Giusti P. Alpha-synuclein and Parkinson's disease. FASEB J. 2004, 18:617-626.
76. Robberecht W., Philips T. The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 2013, 14:248-264.
77. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
78. Ruan Q., Harrington A.J., Caldwell K.A., Caldwell G.A., Standaert D.G. VPS41, a protein involved in lysosomal trafficking, is protective in Caenorhabditis elegans and mammalian cellular models of Parkinson's disease. Neurobiol. Dis. 2010, 37:330-338.
79. Samann J., Hegermann J., von Gromoff E., Eimer S., Baumeister R., Schmidt E. Caenorhabditis elegans LRK-1 and PINK-1 act antagonistically in stress response and neurite outgrowth. J. Biol. Chem. 2009, 284:16482-16491.
80. Sangha J.S., Sun X., Wally O.S., Zhang K., Ji X., Wang Z., Wang Y., Zidichouski J., Prithiviraj B., Zhang J. Liuwei Dihuang (LWDH), a traditional Chinese medicinal formula, protects against beta-amyloid toxicity in transgenic Caenorhabditis elegans. PLoS One 2012, 7:e43990.
81. Settivari R., Levora J., Nass R. The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in caenorhabditis elegans models of manganism and parkinson disease. J. Biol. Chem. 2009, 284:35758-35768.
82. Settivari R., Vanduyn N., Levora J., Nass R. The Nrf2/SKN-1-dependent glutathione S-transferase pi homologue GST-1 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of manganism. Neurotoxicology 2013, 38:51-60.
83. Silva M.C., Fox S., Beam M., Thakkar H., Amaral M.D., Morimoto R.I. A genetic screening strategy identifies novel regulators of the proteostasis network. PLoS Genet. 2011, 7:e1002438.
84. Springer W., Hoppe T., Schmidt E., Baumeister R. A Caenorhabditis elegans Parkin mutant with altered solubility couples alpha-synuclein aggregation to proteotoxic stress. Hum. Mol. Genet. 2005, 14:3407-3423.
85. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de Belleroche J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
86. Steinkraus K.A., Smith E.D., Davis C., Carr D., Pendergrass W.R., Sutphin G.L., Kennedy B.K., Kaeberlein M. Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 2008, 7:394-404.
87. Su L.J., Auluck P.K., Outeiro T.F., Yeger-Lotem E., Kritzer J.A., Tardiff D.F., Strathearn K.E., Liu F., Cao S., Hamamichi S., Hill K.J., Caldwell K.A., Bell G.W., Fraenkel E., Cooper A.A., Caldwell G.A., McCaffery J.M., Rochet J.C., Lindquist S. Compounds from an unbiased chemical screen reverse both ER-to-Golgi trafficking defects and mitochondrial dysfunction in Parkinson's disease models. Dis. Model. Mech. 2010, 3:194-208.
88. Tauffenberger A., Chitramuthu B.P., Bateman A., Bennett H.P., Parker J.A. Reduction of polyglutamine toxicity by TDP-43, FUS and progranulin in Huntington's disease models. Hum. Mol. Genet. 2013, 22:782-794.
89. Treusch S., Hamamichi S., Goodman J.L., Matlack K.E., Chung C.Y., Baru V., Shulman J.M., Parrado A., Bevis B.J., Valastyan J.S., Han H., Lindhagen-Persson M., Reiman E.M., Evans D.A., Bennett D.A., Olofsson A., DeJager P.L., Tanzi R.E., Caldwell K.A., Caldwell G.A., Lindquist S. Functional links between Abeta toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 2011, 334:1241-1245.
90. Usenovic M., Knight A.L., Ray A., Wong V., Brown K.R., Caldwell G.A., Caldwell K.A., Stagljar I., Krainc D. Identification of novel ATP13A2 interactors and their role in alpha-synuclein misfolding and toxicity. Hum. Mol. Genet. 2012, 21:3785-3794.
91. Vaccaro A., Tauffenberger A., Aggad D., Rouleau G., Drapeau P., Parker J.A. Mutant TDP-43 and FUS cause age-dependent paralysis and neurodegeneration in C. elegans. PLoS One 2012, 7:e31321.
92. Vaccaro A., Tauffenberger A., Ash P.E., Carlomagno Y., Petrucelli L., Parker J.A. TDP-1/TDP-43 regulates stress signaling and age-dependent proteotoxicity in Caenorhabditis elegans. PLoS Genet. 2012, 8:e1002806.
93. Valente E.M., Salvi S., Ialongo T., Marongiu R., Elia A.E., Caputo V., Romito L., Albanese A., Dallapiccola B., Bentivoglio A.R. PINK1 mutations are associated with sporadic early-onset Parkinsonism. Ann. Neurol. 2004, 56:336-341.
94. Valentine J.S., Doucette P.A., Zittin Potter S. Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem. 2005, 74:563-593.
95. van Ham T.J., Thijssen K.L., Breitling R., Hofstra R.M., Plasterk R.H., Nollen E.A. C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. PLoS Genet. 2008, 4:e1000027.
96. Vance C., Rogelj B., Hortobagyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., Ganesalingam J., Williams K.L., Tripathi V., Al-Saraj S., Al-Chalabi A., Leigh P.N., Blair I.P., Nicholson G., de Belleroche J., Gallo J.M., Miller C.C., Shaw C.E. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
97. Vanduyn N., Settivari R., Wong G., Nass R. SKN-1/Nrf2 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of methylmercury toxicity. Toxicol. Sci. 2010, 118:613-624.
98. VanDuyn N., Settivari R., LeVora J., Zhou S., Unrine J., Nass R. The metal transporter SMF-3/DMT-1 mediates aluminum-induced dopamine neuron degeneration. J. Neurochem. 2013, 124:147-157.
99. Vartiainen S., Pehkonen P., Lakso M., Nass R., Wong G. Identification of gene expression changes in transgenic C. elegans overexpressing human alpha-synuclein. Neurobiol. Dis. 2006, 22:477-486.
100. Ved R., Saha S., Westlund B., Perier C., Burnam L., Sluder A., Hoener M., Rodrigues C.M., Alfonso A., Steer C., Liu L., Przedborski S., Wolozin B. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J. Biol. Chem. 2005, 280:42655-42668.
101. Wang H., Lim P.J., Yin C., Rieckher M., Vogel B.E., Monteiro M.J. Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin. Hum. Mol. Genet. 2006, 15:1025-1041.
102. Wang H., Lim P.J., Karbowski M., Monteiro M.J. Effects of overexpression of huntingtin proteins on mitochondrial integrity. Hum. Mol. Genet. 2009, 18:737-752.
103. Wang J., Farr G.W., Hall D.H., Li F., Furtak K., Dreier L., Horwich A.L. An ALS-linked mutant SOD1 produces a locomotor defect associated with aggregation and synaptic dysfunction when expressed in neurons of Caenorhabditis elegans. PLoS Genet. 2009, 5:e1000350.
104. Wang P., Lazarus B.D., Forsythe M.E., Love D.C., Krause M.W., Hanover J.A. O-GlcNAc cycling mutants modulate proteotoxicity in Caenorhabditis elegans models of human neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17669-17674.
105. Wood-Kaczmar A., Gandhi S., Wood N.W. Understanding the molecular causes of Parkinson's disease. Trends Mol. Med. 2006, 12:521-528.
106. Wroe R., Wai-Ling Butler A., Andersen P.M., Powell J.F., Al-Chalabi A. ALSOD: the Amyotrophic Lateral Sclerosis Online Database. Amyotroph. Lateral Scler. 2008, 9:249-250.
107. Wu Y., Cao Z., Klein W.L., Luo Y. Heat shock treatment reduces beta amyloid toxicity in vivo by diminishing oligomers. Neurobiol. Aging 2010, 31:1055-1058.
108. Wu C.H., Fallini C., Ticozzi N., Keagle P.J., Sapp P.C., Piotrowska K., Lowe P., Koppers M., McKenna-Yasek D., Baron D.M., Kost J.E., Gonzalez-Perez P., Fox A.D., Adams J., Taroni F., Tiloca C., Leclerc A.L., Chafe S.C., Mangroo D., Moore M.J., Zitzewitz J.A., Xu Z.S., van den Berg L.H., Glass J.D., Siciliano G., Cirulli E.T., Goldstein D.B., Salachas F., Meininger V., Rossoll W., Ratti A., Gellera C., Bosco D.A., Bassell G.J., Silani V., Drory V.E., Brown R.H., Landers J.E. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012, 488:499-503.
109. Zhang T., Mullane P.C., Periz G., Wang J. TDP-43 neurotoxicity and protein aggregation modulated by heat shock factor and insulin/IGF-1 signaling. Hum. Mol. Genet. 2011, 20:1952-1965.